Alexandra Pereira da Silva 1* & Rogério Vieira Rossi 1

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1 New records of Vampyrum spectrum (Chiroptera, Phyllostomidae) for the Pantanal domain in Brazil, with notes on the species natural history, biometry, and lower incisors arrangement Alexandra Pereira da Silva 1* & Rogério Vieira Rossi 1 1. Instituto de Biociências, Universidade Federal de Mato Grosso, Avenida Fernando Correa da Costa, 2367, CEP , Cuiabá, Mato Grosso, Brazil. * Corresponding author. drisanainlua@gmail.com Abstract Vampyrum spectrum is the largest bat of the New World, with wingspan reaching up to one meter. This carnivorous bat has wide geographical distribution that extends from the state of Veracruz, Mexico, to central Brazil and northern Bolivia. To date, 21 specimens have been recorded in Brazil, most of them in the Amazonian domain. There is only one record for the species in the Pantanal domain, referring to a specimen collected in 1944 in Barra do Aricá, State of Mato Grosso. In this study we present two new records of V. spectrum for the Pantanal domain, in the Poconé region, State of Mato Grosso, constituting the second and third records of the species for this region after more than 50 years with no local records. Our records represent the southern limit of the species range in Brazil and raise to 23 the number of records in the country. Data on the natural history, biometry, and lower incisors arrangement of the collected specimens are provided. Keywords: False vampire, Vampyrum, morphology, geographic distribution, Pantanal. Introduction The false vampire bat, Vampyrum spectrum (Linnaeus, 1758), is the largest bat of the New World, with wingspan that reaches up to one meter and body mass of up to 190 g (Navarro & Wilson 1982; Nowak 1994). The species has a predominantly carnivorous habit and is considered a top predator (Vehrencamp et al. 1977; Emmons & Feer 1997), needing a large foraging area, which probably accounts for its generally low local density (Bernard & Fenton 2002). According to the information available in the literature, V. spectrum has a wide geographical distribution that extends from the state of Veracruz, Mexico, to central Brazil and northern Bolivia (Emmons & Feer 1997; Williams & Genoways 2007; Reid 2009). Most Brazilian records of this taxon are from the Amazonian domain, where it is widely distributed despite its low density at several study sites. In this sense, from the 21 specimens already recorded in Brazil seven are from the State of Amazonas (Piccinini 1974; Reis & Guillaumet 1983; Reis 1984; Reis & Peracchi 1987; Sampaio et al. 2003), six from the State of Pará (Bernard 2001; Kalko & Handley 2001; Bernard & Fenton 2002;), and three from the State of Amapá (Peracchi et al. 1984; Martins et al. 2006), while the states of Acre and Rondônia have one record each (Nogueira et al. 1999; Discher et al. 2009). In the Cerrado domain, a specimen was captured in the State of Tocantins (Nunes et al. 2005); and in the Caatinga domain, a specimen was captured in the State of Piauí (Gregorin et al. 2008), which is the easternmost record for Brazil. There is only one record for the species in the Pantanal domain, collected in 1944 from Barra do Aricá, State of Mato Grosso (Marinho-Filho & Sazima 1998; Vieira 1945) (Figure 1). Figure 1 Previous records (circles) and present study records (square) of Vampyrum spectrum in Brasil. The aim of this study is to present two new records of V. spectrum for the Pantanal domain, in the Poconé region, State of Mato Grosso, constituting the second and third records of the species for this seasonally flooded biome after 836

2 Chiroptera Neotropical 17(1), July 2011 more than 50 years without any records for the region. Our records represent the southern limit of the species range in Brazil and raise to 23 the number of records of V. spectrum in the country. Material and Methods Two individuals of V. spectrum were captured during a bat inventory program held in Pirizal District, Municipality of Nossa Senhora do Livramento, Poconé region, State of Mato Grosso, Brazil, between June and August 2006, under the auspices of the project Meso-scale patterns of Biodiversity in the Different Pastoral Systems of the Pantanal in the State of Mato Grosso (BIOPAN), conducted by the Pantanal Research Center (CPP). The collection sites belong to a long-term sampling site which consists of a RAPELD sampling system described by Magnusson et al. (2005), made up of thirty 250-mlong plots systematically distributed over a 25 km2 area. The plots are equidistant, spaced 1 km apart and follow the topography of the terrain (Figure 2). Specimens of V. spectrum were captured in mist nets (12m x 2.5m, 22.0 mm mesh), arranged in a continuous 108-m-line at two collection points (plot D2 = 16º S, 56º W; plot D4 = 16º S, 56º W), 2 km away from each other (Figure 2). Individuals were placed in cloth bags, weighed, measured and their reproductive condition assessed. They were subsequently euthanized, fixed in 10% formaldehyde and preserved in 70% alcohol. In the laboratory, the skulls were removed and cleaned with the help of carrion beetles of the genus Dermestes. Eleven craniodental measurements were taken with digital calipers to the nearest 0.01 mm, based on the procedures in Simmons & Voss (1998) and Vizotto & Taddei (1973). The stomachs of both specimens were examined to verify any food items consumed. These specimens (UFMT ) are deposited in the Coleção Zoológica da Universidade Federal de Mato Grosso, Cuiabá, State of Mato Grosso, Brazil. Figure 2 Study grid in Pirizal District, Poconé region, State of Mato Grosso, Brazil, showing the sampling points (A1 to F5). The circles represent the sampling points where specimens of Vampyrum spectrum were captured. 837

3 Results and Discussion The first individual, an adult male with abdominal testis, was captured on August 10, 2006 in a pasture environment on a seasonally flooded forest, composed predominantly of the plant Vochysia divergens (Pohl, Vochysiaceae) (Nunes da Cunha et al. 2007). There is a permanent lake in the site, which is full even during the dry season. The second individual, a lactating female with complete dentition and body dimensions slightly larger than the male (Table 1), was captured on August 12, 2006 in a seasonally flooded savanna environment with termite mounds, also called murundu fields in the Pantanal. The predominant plant species were V. divergens and Curatella americana (L., Dilleniaceae). The information presented in this report is congruent with that found by Acosta & Azurdy (2006) in Bolivia regarding the time of capture and the time of year when females with signs of lactation were captured. Characteristics observed at the capture sites of the present study, such as typically open environments, presence of permanent water bodies, and proximity to human dwellings match those described for most of the records from the Amazon region and from Bolivia (Vehrencamp et al. 1977; Bernard & Fenton 2002; Acosta & Azurdy 2006; Discher et al. 2009). Table 1 Reproductive condition, body measurements (in millimeters), body mass (in grams), and time of capture of specimens of Vampyrum spectrum in the present study. The measurements follow Simmon and Voss (1998). External measurements UFMT 1116 UFMT 1117 and natural history data Reproductive condition Male, abdominal testis Female, lactating Forearm length Foot length Ear length Thumb length Tibia length Weigth Time of capture 19h33min 20h55min The stomachs of both specimens were empty. Body measurements of both specimens showed intermediate values compared to those found by Husson (1978) and Simmons & Voss (1998) for specimens from Suriname and Paracou (French Guyana) respectively, and similar values to the specimens from Bolivia (Vargas-Espinoza et al. 2004; Acosta & Azurdy 2006). Moreover, as mentioned earlier, we recorded slightly larger body measurements in the female (Table 1). Husson (1978) found no major differences in the external measurements of the three males and two females he analyzed. On the other hand, Simmons & Voss (1998) recorded larger forearms and feet in two males compared to a single female specimen, and Vargas-Espinoza et al. (2004) reported considerably larger ears in two males when compared to three females. In another study of V. spectrum in Bolivia, Acosta & Azurdy (2006) observed that the external measurements of a female specimen were slightly larger than those of the male, similar to the results presented herein. Few records of craniodental measurements for V. spectrum can be found in the literature, and this study presents the first cranial and dental measurements for this species in Brazil (Table 2). In general, measurements of the individuals captured in this study are larger than those of specimens examined by Simmons & Voss (1998) and Husson (1978). An exception is the maxillary toothrow length, which is larger in the specimens examined by the latter author. Unlike the body measurements, we found that most craniodental measurements are slightly larger in the male. This same pattern was not found by Simmons & Voss (1998) and Husson (1978) in specimens from Paracou (French Guyana) and Surinam respectively. Both specimens collected in this study have full dentition and complete ossification of the metacarpals, and therefore may be considered adults. However, the teeth of the female specimen are quite worn, and the apex of the lower canine is broken, which suggests that it is an older animal. The male specimen, on the other hand, has no tooth wear, suggesting that this is a younger specimen, which could explain the slightly smaller body dimensions when compared to those of the female. 838

4 Table 2 - Craniodental measurements (in millimeters) of the specimens of Vampyrum spetrum collected in the present study. The measurements follow Simmons and Voss (1998), except when otherwise mentioned. a Based on Vizotto and Taddei (1973). Craniodental measurements UFMT 1116 (male) UFMT 1117 (female) Greatest length of skull Condyloincisive length a Condylocanine length a Lacrimal breadth Postorbital breadth Zygomatic breadth Braincase breadth Mastoid breadth Maxillary toothrow length Breadth across molars Breadth across canines Another characteristic observed in the dentition of our specimens that deserves to be mentioned is the disposition of the lower incisors. The female has a row of four lower incisors aligned between the canines, while the two lower external incisors of the male are positioned below the internal ones, probably due to the lack of space between the canines which cannot maintain the four incisors in a row (Figure 3). Navarro & Wilson (1982) described the pattern of incisor arrangement in V. spectrum as the inner pair located behind the outer pair, as observed in the male specimen of this study. However, Husson (1978) illustrated lower incisors aligned between the canines, as observed in the female specimen from Pirizal. On analyzing three specimens of V. spectrum deposited in the Museu de Zoologia da Universidade de São Paulo (MZUSP 6493, 12946, 33556) and other two specimens to be deposited in the same institution (field numbers N3Q3.004 and PIQ 53), we found that the lower incisors of V. spectrum showed different levels of alignment, of which the extreme patterns corresponds to those observed in the two specimens collected by us (Figure 3). Figure 3 Frontal view of the mandibules of Vampyrum spectrum specimens collected in the present study. Note the different patterns of the lower incisors alignment in the female (A) and male (B) specimens. Photographed by Thiago Semedo. Acknowledgements We thank the Pantanal Research Center (CPP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support and research grant awarded to APS. We also thank Christine Strussmann for logistical support in the 839 field, and the Pantanal guides and trainees who assisted in field work. We thank Cleuton Lima Miranda for suggestions and criticisms on earlier drafts of this manuscript, and Thiago Semedo for helping with the photograph and distribution map editions. We also thank Mario de Vivo for

5 allowing access to the specimens housed in the MZUSP, and Juliana Gualda for help examining the specimens from the museum. References Acosta L. & Azurduy H Primeras colectas del Falso Vampiro Vampyrum spectrum (Phyllostomidae, Chiroptera) en el sector sur del Bosque Seco Chiquitano, Santa Cruz, Bolivia. Kempffiana 2: Bernard E Species list of bats (Mammalia: Chiroptera) of Santarém area, Pará State, Brazil. Revista Brasileira de Zoologia 18: Bernard E. & Fenton M.B Species diversity of bats (Mammalia: Chiroptera) in forest fragments, primary forests and savannas in central Amazonia, Brazil. Canadian Journal of Zoology 80: Discher D.S.; Bernard P.S. & Facure K.G Mammalia, Chiroptera, Phyllostomidae, Vampyrum spectrum (Linnaeus, 1758): First record for the state of Rondônia, Brazil, and new prey records. Check List 5: Emmons L.H. & Feer F Neotropical rainforest mammals: a field guide. Second edition. University of Chicago Press, Chicago. Gregorin R.; Carmignotto A.P. & Percequillo A.R Quirópteros do Parque Nacional da Serra das Confusões, Piauí, nordeste do Brasil. Chiroptera Neotropical 14: Husson A.M The mammals of Suriname. Zoölogische Monographieën van het Rijksmuseum van Natuurlijke Historie, No 2. Leiden: E. J. Brill. Kalko E.K.V. & Handley-Jr C.O Neotropical bats in the canopy: diversity, community structure, and implications for conservation. Plant Ecology 153: Magnusson W.E.; Lim A.P.; Luizão R.; Luizão F.; Costa F.R.C.; Castilho C.V. & Kinupp V.F RAPELD: Uma modificação do método de Gentry para o levantamento da biodiversidade em áreas. Biota Neotropica 5: 1-6. Marinho-Filho J. & Sazima I Brazilian bats and conservation biology: a first survey. In: Bat biology and conservation (edited by Kunz T.H. & Racey P.A.), pp , Smithsonian Institution Press, Washington, D.C. Martins A.C.M.; Bernard E. & Gregorin R Inventários biológicos rápidos de morcegos (Mammalia, Chiroptera) em três unidades de conservação do Amapá, Brasil. Revista Brasileira de Zoologia 23: Navarro L. & Wilson D.E Vampyrum spectrum. Mammalian Species 184: 1-4. Nogueira M.R.; Pol A. & Peracchi A.L New records of bats from Brazil with a list of additional species for the chiropteran fauna of the state of Acre, western Amazon basin 840 (Mammalia, Chiroptera). Mammalia 63: Nowak R.M Walker s Bats of the world. John Hopkins University Press, Baltimore. Nunes A.; Marques-Aguiar S.; Saldanha N.; Silva R.S. & Bezerra A New records on the geographic distribution of bat species in the Brazilian Amazonia. Mammalia 69: Nunes da Cunha C.; Junk W.J. & Leitão-Filho H Woody Vegetation in the Pantanal of Mato Grosso, Brazil: a Preliminary Tipology. Amazoniana 19: Peracchi A.L.; Raimundo S.D.L. & Tannure A.M Quirópteros do Território Federal do Amapá, Brasil (Mammalia, Chiroptera). Arquivos da Universidade Federal Rural do Rio de Janeiro 7: Piccinini R.S Lista provisória dos quirópteros da coleção do Museu Paraense Emilio Goeldi (Chiroptera). Boletim do Museu Paraense Emilio Goeldi, Nova Série Zoológica 77: Reid F.A A Field Guide to the Mammals of Central America and Southeast Mexico. Second edition. Oxford University Press, New York. Reis N.R Estrutura de comunidades de morcegos na região de Manaus, Amazonas. Revista Brasileira de Biologia 44: Reis N.R. & Peracchi A.L Quirópteros da região de Manaus, Amazonas, Brasil (Mammalia, Chiroptera). Boletim do Museu Paraense Emilio Goeldi, Nova Série Zoológica 3: Reis N.R. & Guillaumet J.-L Les chauvessouris frugivores de la région de Manaus et leur rôle dans la dissémination des espèces végétales. Revue D Ecologie La Terre Et La Vie 38: Sampaio E.M.; Kalko E.K.V.; Bernard E.; Rodriguez-Herrera B. & Handley-Jr C.O A biodiversity assessment of bats (Chiroptera) in a tropical lowland rainforest of Central Amazonia, including methodological and conservation considerations. Studies on Neotropical Fauna and Environment 38: Simmons N.B. & Voss R.S The mammals of Paracou, French Guiana: a Neotropical lowland rainforest fauna. Part I. Bats. Bulletin of the American Museum of Natural History 237: Vargas-Espinoza A.; Aguirre L.F.; Swarner M.; Emmons L. & Teran M Distribución de Vampyrum spectrum em Bolívia y comentarios sobre su estado de conservación. Ecología em Bolivia 39: Vehrencamp S.L.; Stiles F.G. & Bradbury J.W Observations on the foraging behavior and avian prey of the Neotropical carnivorous bat, Vampyrum spectrum. Journal of Mammalogy 58:

6 Vieira C.C Sobre uma coleção de mamíferos de Mato Grosso. Arquivos de Zoologia do Estado de São Paulo 4: Vizzoto L.D. & Taddei V.A Chave para a determinação de quirópteros brasileiros. Revista da Faculdade de Filosofia, Ciências e Letras de São José do Rio Preto - Boletim de Ciências 1: 1-72p. Williams S.L. & Genoways H.H [2007]. Subfamily Phyllostominae Gray, In: Mammals of South America. Volume 1. Marsupials, Xenarthrans, Shrews, and Bats (edited by Gardner A.L.), pp , University of Chicago Press, Chicago. 841

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